[visually familiar faces (VFF), which were seen
hundreds of times by the subjects before the experiments; see SM for details], whereas the others
were completely unfamiliar [nonfamiliar faces
(NFF)]. We generated analogous stimulus categories for objects: visually familiar objects (VFO), seen
as much as VFF, and nonfamiliar objects (NFO),
and defined an object-selective area to explore familiarity effects for these categories (see SM and
fig. S3). We analyzed the effect of visual and personal familiarity as the modulation in activity
relative to unfamiliar stimuli (contrast VFF/O >
NFF/O and PFF/O > NFF/O, normalized to face/
object selectivity) with a region of interest (ROI)
analysis (see SM). Visual and personal familiarity systematically modulated the activity of individual face and object areas (Fig. 2, D and E,
and fig. S2) and in larger groups of areas (core
face areas, new anterior temporal areas, prefrontal areas, and an object-selective area) (Fig.
2F). Visual familiarity with faces and objects re-
duced activity significantly in many, but not all,
face and object areas (Fig. 2, D and F). Personal
familiarity with faces enhanced activity in all face
areas and groups, whereas personal familiarity
with objects reduced activity in the object area
(Figs. 2, E and F, and fig. S2). Thus, the main
effects of familiarity were activity enhancement
of personal familiarity in face areas (Fig. 2F) (P <
0.01, without significant differences in modula-
tion between the three groups of face areas) and
general activity reduction of responses to famil-
iar objects (Fig. 2F and fig. S2). Effects of famil-
iarity are widespread throughout face and object
selective areas; they can be strong, enhancing, or
suppressing, and they are highly specific, depend-
ing on an interaction between local specialization,
stimulus category, and the nature of familiarity
(Fig. 3F) (three-way ANOVA interaction effect,
F(3,48) = 2.79, P = 0.05).
A hallmark of familiar face processing is efficient recognition even during partial occlusion
or severe blurring (29, 30). Under these conditions,
face information might be processed for a long
time before a sudden transition to recognition.
A paradigm sensitive to this signature has recently
been introduced (31). Here, initially highly blurred
and unrecognizable stimuli slowly incorporate,
over the course of seconds, increasing amounts
of high spatial frequency (HSF) information (Fig. 3A).
With this type of stimulation, activity in generic
face- and object-processing systems is expected
to increase linearly, in parallel to information accumulation. Instead, familiar face-recognition systems are expected to (additionally) nonlinearly
accelerate activation upon recognition (31) (Fig. 3B).
We used three sets of stimuli—personally familiar
faces, unfamiliar faces, and objects—which were
revealed over the course of 32 s (see SM). Activity
in the core face areas and in face area PV (
prefrontal ventral) ramped up concomitantly, exhibiting an advantage of faces over nonface objects
and of personally familiar over unfamiliar faces
throughout the stimulation period (Fig. 3C). Response time courses in face area PO (prefrontal
orbital) differed markedly, exhibiting a face familiarity preference early on, and maintained
throughout stimulation. This pattern of results is
compatible with the hypothesis that PO uses low
spatial frequency information to form a “first
guess” of stimulus identity (32). Face areas TP and
PR, however, exhibited a highly nonlinear response
increase, and this accelerated response increment
occurred for PFF only. TP was not even activated
by any of the other stimuli (permutation tests
592 11 AUGUST 2017 • VOL 357 ISSUE 6351 sciencemag.org SCIENCE
Fig. 1. Organization of face-processing system in the
rhesus macaque for unfamiliar faces and hypotheses
for familiar face processing.
(A) Schematic of the macaque
face-processing system (10).
Core network: areas PL (
posterior lateral), ML (middle lateral), MF (middle fundus), MD
(middle dorsal) (17), AL (
anterior lateral), AF (anterior fundus), AD (anterior dorsal (12),
in the superior temporal sulcus
(sts), and the anterior medial
face area (AM) on the ventral
surface of the temporal lobe.
Extended prefrontal network
(11): area PO (prefrontal
orbital), in the lateral orbital
sulcus, PA (prefrontal arcuate),
and PV [prefrontal ventral,
corresponding to PL in (11)].
Prefrontal areas can be modulated by facial expression (11).
ls, lateral sulcus. (B) Three
hypothetical scenarios for
familiar face processing. Differential responses are
depicted in a darker tint.
(a) Modulation by familiarity
in the face-processing system. It can either increase or decrease
activity. (b) An anterior-posterior gradient of modulation, with identity-selective representations particularly selective for familiar faces.
Activity increases with familiarity in the more anterior face-selective
areas, as other qualities do (15, 42). (c) Familiar face processing relies
on additional brain areas outside the core face-processing system.
Although the core system does not differentiate between familiar
and unfamiliar faces, an extended face system exists that is highly
selective for familiar faces. The extended system could code for
familiarity in a distributed or modular manner. In a distributed
system, neurons carry information for multiple stimulus categories.
In a modular system, each neuron within the area carries information
relevant to only one category: familiar faces or objects. (C) Activation
maps of the group (fixed effects) analysis showing regions significantly
more activated by faces than control objects overlaid on the partially
inflated right hemisphere of M1’s brain. Color-scale indicates negative
common logarithm of P value, corrected for multiple comparisons
(FDR, q < 0.05).